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http://bioscience.oxfordjournals.org September 2014 / Vol. 64 No. 9 • BioScience 789

Effects of Oil Spills on Terrestrial Arthropods in Coastal Wetlands

STEVEN C. PENNINGS, BRITTANY D. McCALL, AND LINDA HOOPER-BUI

Coastal wetlands are important to human well-being and vulnerable to oil spills. Research on biotic effects of oil has been focused on microbes, plants, and benthic invertebrates, neglecting terrestrial arthropods. We review how oil affects terrestrial arthropods in coastal marshes and suggest future research topics. Terrestrial arthropods play important ecological roles in coastal marshes, affecting primary production and decomposition and providing food to terrestrial and marine vertebrates. Some species are pests and disease vectors for humans and livestock. Terrestrial arthropods are sensitive to oil exposure and are suppressed even in lightly oiled sites where plants are not affected. Some arthropods later reinhabit oiled marshes, which demonstrates that portions of the arthropod community may be resilient to oil exposure. However, oil that remains in sediments may affect terrestrial populations for years after the spill. The sensitivity of arthropods to oil exposure makes them useful indicators of marsh health following environmental impacts.

Keywords: Deepwater Horizon, insects, Macondo, oil spill, salt marsh

Coastal salt marshes, although they occupy a small area of the globe, provide numerous ecosystem ser-

vices to humanity, such as supporting recreationally and commercially important food webs, moderating coastal disturbances, storing carbon and nitrogen, and transforming nutrients (Costanza et al. 1997, Pennings and Bertness 2001, Barbier et al. 2011, Shepard et al. 2011, Spencer and Harvey 2012). In a number of studies, the threats that oil spills pose to these habitats have been examined; however, these studies have been focused on some taxa, particularly soil microbes, plants, and benthic invertebrates, and others have been neglected. Here, we review what little is known about how oil spills affect the terrestrial arthropod community in salt marshes and identify areas in which future research is needed (figure 1).

Oil spills represent a major environmental threat to coastal marshes, because these marshes are low-energy and anoxic environments; therefore, the dispersal and decomposition of oil are slow, and oil may persist within the soil for decades (Teal and Howarth 1984, Hester and Mendelssohn 2000, Peacock et al. 2005). This persistent oil may have long-lasting effects on flora and fauna and may impede the recovery of the system (Culbertson et al. 2007, 2008). There are well-documented impacts of oil contamination on salt marsh soil properties, infauna, and plant populations (Decker and Fleeger 1984, Pezeshki et al. 2000, Pezeshki and DeLaune 2002, DeLaune et al. 2003, Mishra et al. 2012, Silliman et al. 2012, Brunner et al. 2013). Benthic invertebrate populations, including resident “marine arthropods,” such as intertidal

crabs and the fish and invertebrate populations that use salt marshes as temporary feeding or nursery grounds, have also received attention (Pezeshki et al. 2000, Andrade et al. 2004, Culbertson et al. 2007, Whitehead et al. 2011). In contrast, there has been almost no study of the effects of oil exposure on the salt marsh terrestrial arthropod community (figure 2), which, for the purposes of this article, we define as Hexapoda (including insects and springtails) and Arachnida (including spiders, mites, and pseudoscorpions).

The importance of terrestrial arthropodsTerrestrial arthropods play an important role in the ecol-ogy of coastal salt marshes (figure 3). They occur at high densities, up to several thousand individuals per square meter (Denno et al. 2000, 2002, 2005, Wimp et al. 2010). The community is not as diverse as those found in terrestrial grasslands because of the low plant diversity of salt marshes, but terrestrial arthropods nevertheless represent a major component of multicellular biodiversity in salt marshes, with 100 or more species in Spartina alterniflora stands alone (Pfeiffer and Wiegert 1981, Wimp et al. 2010). Similar levels of species richness can be found in stands of other salt marsh plant species, such as Juncus roemerianus and Distichlis spicata (Rey and McCoy 1997). Other insects are abundant in wet sediments or marsh pools (Campbell and Denno 1978, Kelts 1979, Ward and FitzGerald 1983, Barnby et al. 1985). The taxonomic composition varies among sites, but, typically, Diptera and Heteroptera (formerly Hemiptera and Homoptera) are most abundant, followed by Coleoptera,

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Collembola, Hymenoptera, Orthoptera, and Thysanoptera (Davis and Gray 1966, Foster and Treherne 1976, Rey and McCoy 1997). This taxonomic diversity provides an extra-ordinary opportunity to explore how vulnerability to oil varies among species as a function of physiology, life history, and microhabitat use.

Terrestrial arthropods affect primary production and nutrient cycling in salt marshes. Herbivorous taxa, such as planthoppers, stem-boring flies and beetles, and grass-hoppers, affect plant growth (Denno et al. 2002, Finke and Denno 2004, Stiling and Moon 2005, Jiménez et al. 2012). Detritivorous taxa, such as Collembola (springtails), affect the transfer of plant primary production into the decomposer food web (Rusek 1998). Predatory taxa, such as spiders, and parasitoids, such as wasps, can affect the densities of both herbivores and detritivores, which indi-rectly affects the rates of herbivory and detritivory (Denno et al. 2002, 2005, Stiling and Moon 2005). Because many of

the ecosystem services provided by salt marshes depend on vigorous plant growth and the decomposition of plant detritus, terrestrial arthropods may play a larger role than is usually realized in mediating salt marsh ecosystem services. How invertebrates affect ecosystem services, however, is not well documented for any habitat type (Prather et al. 2013), including salt marshes, and so the magnitude of this role remains to be determined.

Terrestrial arthropods provide valuable nutrient linkages that connect disparate parts of the ecosystem. In particular, terrestrial arthropods represent an important trophic link to both terrestrial and marine vertebrates. Both migratory birds, such as painted buntings, and marsh residents, such as seaside sparrows, feed on a variety of insects and spiders associated with marsh plants (Pfeiffer and Wiegert 1981, Brittain et al. 2012). Some passerine birds pick the insects off the exterior of the plants (Kale 1964, Brittain et al. 2012), whereas others drill into the plants and consume

Figure 1. Oiled marsh at Barataria Bay, Louisiana, in 2010. The Spartina alterniflora grasses at the leading edge of the marsh were heavily coated with oil and have died. A floating boom intended to keep oil out of the marsh has washed into the marsh and is contributing to crushing oiled vegetation. Behind the heavily oiled area, lightly oiled S. alterniflora appears healthy, but does it support a functioning arthropod community? Photograph: Steven C. Pennings.



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2013). A number of mosquitoes, biting gnats, and biting flies pass through their larval stages in marsh muds and ponds (Axtell 1976). These species can represent a major irritant to humans and livestock and can spread malaria, heartworm, filariasis, encephalitis, and other diseases (Axtell 1976, Linley 1976, O’Meara 1976). Efforts to control these taxa, especially mosquitoes, have led to widespread human modification (ditches or impoundments) of marsh habitats (Daiber 1986, Crain et al. 2009, Gedan et al. 2009).

Responses of terrestrial arthropods to oil spillsThe work to date suggests that terrestrial arthropods might be more sensitive to oil exposure than are plants (McCall and Pennings 2012). Following the BP Deepwater Horizon’s Macondo oil spill, McCall and Pennings (2012) sampled replicated sites in Louisiana and Mississippi in August 2010 and 2011. Some sites were exposed to oil; reference sites showed no visible signs of oil. The oiled sites typically had a band of heavily oiled dead S. alterniflora up to 5 meters (m) wide at the leading edge of the marsh (Silliman et al. 2012, Michel et al. 2013). McCall and Pennings (2012) sampled terrestrial arthropods 1–2 m behind this band, in stands of S. alterniflora that appeared healthy, despite some oil on the soil surface and bases of the plant stems. Abiotic conditions, such as soil organic content, water content, and soil salinity, and plant variables such as height, the percentage cover of live plants, and the percentage cover of dead plant material did not differ between the oiled and the control sites. S. alter-niflora leaf nitrogen content, however, was higher at the oiled sites, for reasons that are not clear.

In this zone of moderate oiling and putatively healthy S. alterniflora plants, the total densities of terrestrial arthropods

Figure 2. Representative arthropods from coastal salt marshes in the United States. (a) Prokelisia sp. planthopper (photograph: Chuan-Kai Ho); (b) Chaetopsis sp. fly whose larvae are stem-boring herbivores; (c) Conocephalus aigialus, an omnivore (photograph: Liz Wason); (d) Hogna sp., a predator; (e) Ischnodemus badius, an herbivore; (f) Chlorochroa senilis, an herbivore; (g) Orchelimum fidicinium, an omnivore; (h) a salticid spider, likely Marpissa sp. Unless specified otherwise, photographs: Jim Sheehan.

stem-boring insects concealed within (Xiong et al. 2010). Many other shorebirds that are not primarily insectivores nevertheless include insects as a component of their diets (Kelts 1979, Pfeiffer and Wiegert 1981, Rey and McCoy 1997).

Terrestrial arthropods are also eaten by multiple spe-cies of estuarine fish (Pfeiffer and Wiegert 1981). Insects often represent 20%–60% of the diet of small estuarine fish (Harrington and Harrington 1961, 1972, Kelts 1979) and can approach 100% of the diet when insects are most abundant (Harrington and Harrington 1961). Insects living on the marsh surface or in pools are most vulnerable to fish predation (Harrington and Harrington 1961), but fish also eat insects that typically avoid being submerged. The Gulf killifish, Fundulus grandis, nudges Spartina stems to knock arthropods onto the water, where it can easily consume them. Small fish such as Fundulus spp. may also jump out of the water to capture insects perching on exposed vegeta-tion (Rey and McCoy 1997). Moreover, as the tide comes in, Prokelisia planthoppers and other insects get caught in the surface tension of the water, which makes them easy prey for fish (Harrington and Harrington 1972, Kneib and Stiven 1978, Rey and McCoy 1997). The smaller fish that feed in the marsh are, in turn, food for larger fish of recreational and commercial importance (Kneib 1997). Therefore, by supporting populations of birds and fish, terrestrial arthro-pods contribute indirectly to supporting a range of coastal industries, including ecotourism (bird watching), hunting, and recreational and commercial fisheries.

In contrast to these beneficial effects, terrestrial arthro-pods in salt marshes also have negative effects on human societies and economies (Linley 1976, Kay and Russell



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were cut in half immediately after the oil came ashore (McCall and Pennings 2012). This effect was broadly similar across five feeding guilds: predators, sucking herbivores, stem-boring herbivores, parasitoids, and detritivores. This result is important because it indicates that terrestrial arthropod densities may be sharply reduced by oil exposure in areas in which plants appear unaffected. In areas with heavy oil exposure, where plants are obliterated and the marsh surface is covered with a layer of tar, there is no ambi-guity about the impacts of an oil spill, but if a lightly oiled marsh supports vigorous plant growth, casual observers or investigators focusing on primary production might easily conclude that the area was unaffected, although marsh func-tion might, in fact, be significantly impaired.

The work to date also suggests that some terrestrial arthro-pods are resilient to oil exposure. McCall and Pennings (2012) resampled their sites a year after oil came ashore and found that the total densities of terrestrial arthropods had completely recovered. The recovery was statistically similar across the five feeding guilds studied, although there were

hints that detritivores had increased in abundance beyond their initial densities, a result that would be consistent with the initial oil exposure’s creating a large pulse of decompos-ing organic matter along the edges of the marshes. The rapid recovery of terrestrial arthropods is important because it suggests that this group of organisms is quite resilient to oil exposure, able to rapidly bounce back even if it is sharply suppressed by the initial oil exposure.

Directions for future researchBefore taking resilience as the last word on the topic, how-ever, we must emphasize how much remains to be under-stood about the responses of the arthropod community to oil exposure. The responses of salt marsh terrestrial arthropods to oil spills are likely to vary as a function of oil exposure and the ecological characteristics of the plant and arthropod community.

Oil exposure is a function of weathering, the amount of oil reaching an area, and the persistence of the oil in the sediments. The circumstances of the Macondo spill allowed extensive weathering of oil prior to contact with the shore-line (Peterson et al. 2012). Spills closer to shore will have more toxic petroleum that is still intact when the oil washes ashore, which could lead to greater and longer-lasting impacts. Oil impacts will also increase with the total amount of oil reaching an area. McCall and Pennings (2012) exam-ined areas with moderate oil exposure and did not examine nearby areas where plants had been completely killed by heavy oil exposure. Obviously, in the latter areas, a natural arthropod assemblage will not recover until the plant com-munity recovers—if then. Recovery in revegetated areas may have unique trajectories, and this remains to be assessed.

Recovery trajectories are likely to differ between areas that are lightly and those that are heavily oiled because of the per-sistence of oil in the soil. Oil persists in marsh soils for years or decades (Teal and Howarth 1984, Peacock et al. 2005, Culbertson et al. 2007, 2008). This residual oil will continue to affect terrestrial arthropods as it volatilizes, is brought to the surface by burrowing organisms or erosion, or affects the quality of plants used as food or habitat. Heavily oiled sites, with a larger amount of oil incorporated into the soil, may represent locations with greater and longer-lasting impacts on the arthropod community. For example, in the case of the Macondo oil spill, two toxic aromatic components of the oil are recalcitrant in the marshes that fringe the northern Gulf of Mexico (Turner et al. 2014b). The aromatic compounds naphthalene and methylnaphthalene, both of which are toxic to insects, have increased a thousandfold in concentration in the sediment in 1000 days since the oil came ashore (Turner et al. 2014). These volatile aromatic components may be released from the sediments into the water when the marsh is inundated by seawater and are released into the air when the marsh is exposed. Under the latter conditions, these compounds can strongly affect the arthropod community.

The responses of salt marsh terrestrial arthropods to oil spills may also vary as a function of ecological characteristics

Springtails

Grasshoppers

Plants

Planthoppers

Decomposing plantmaterials

Spiders

Fishes

Birds

Figure 3. Terrestrial arthropods play an important role in mediating ecological processes and supporting higher trophic levels in the salt marsh. Herbivorous taxa, such as planthoppers and grasshoppers, affect plant biomass. Detritivorous taxa, such as springtails, affect the decomposition of dead plant material. All of these, plus arthropod predators, such as spiders, are eaten by insectivorous birds and small fish. Graphic: John Norton.



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of the plant and arthropod community. Most of the work to date on oil impacts on terrestrial arthropods has been done in stands of S. alterniflora. Although this is the most abundant salt marsh plant along most of the Gulf and Atlantic coasts of the United States, other species, such as Spartina patens and Juncus spp., are equally or more abundant in some locations, and there is evidence that oiling has a more severe impact on some of these other plant species than on S. alterniflora (Lin and Mendelssohn 2012). Even if S. alterniflora marshes are resilient to moderate oiling, marshes dominated by other plant species—and their associated arthropods—may not be.

The effects of oil exposure are also likely to vary among arthropod species. For example, species that live on the soil surface or low in the canopy, such as hunting spiders and Collembola, are likely to be exposed to more oil (either as liquid or as volatiles) than are species that live high in the plant canopy, such as planthoppers or web-building spiders. Similarly, the terrestrial arthropods occupying wet sediments and marsh ponds will be more exposed to oil than those living in the vegetation canopy above and, therefore, will likely be more affected. (In fact, applications of diesel oil were historically used in Florida to control salt marsh mosquitoes by suffocating the larvae [Foster and Treherne 1976].) In addition, arthropod species will differ in how eas-ily they can recolonize disturbed patches, with those that can fly likely recolonizing faster than those that cannot (Denno 1994, Lundberg and Moberg 2003, Armitage et al. 2013).

We currently know little about the survival of arthropods that recolonize oiled patches. It is possible that arthropods colonizing oiled patches have a high mortality rate because of residual oil, in which case the previously oiled patches would be ecological traps. In other words, a natural density of arthropods might not indicate a healthy ecosystem if the arthropods are dying at a high rate and simply being replaced by unsuspecting migrants that will soon share the same fate. In the same way, sea otter subpopulations in Alaska that inhabit areas with significant residual oil from the Exxon Valdez spill continued to act as sinks on the over-all population for at least 15 years after the spill, with chronic mortality equaling the initial acute mortality at the time of the spill (Monson et al. 2011).

Finally, the dynamics of the recolonization of a disturbed patch almost certainly depend on the landscape cover and arrangement of patches that are heavily, lightly, and not oiled (Denno 1994). In particular, if extensive stands of marshes in a particular area were oiled and no healthy marsh remained in the immediate area, there would be no local source of arthropods to recolonize the disturbed areas.

These points essentially lay out a research agenda for future work on the effects of oil on terrestrial arthropods in coastal wetlands. As this essay has made clear, we currently know very little about this topic, and great uncertainties remain. Continued sampling of salt marsh arthropod communities is needed in order to better characterize these communities and to understand what can be lost following an oil spill or other environmental insult. Mesocosm experiments will be

useful in teasing apart details about how different arthropod species respond to and recover from various oiling scenarios. Investigations into oil dosage and weathering and how plant recovery and microbial biodegradation affect arthropod resil-ience will lend valuable insights into the mechanisms behind functional recovery of the entire system. Additional field studies will be crucially important in testing hypotheses about landscape processes and for transferring laboratory results to more-realistic conditions. In particular, although heavily oiled sites typically receive the most attention, we suggest that more attention needs to be paid to lightly oiled sites, which are more common, especially with the passage of time after the initial spill (Michel et al. 2013). Because terrestrial arthropods appear to be more sensitive to oil exposure than salt marsh plants, many scenarios of oil exposure could create salt marshes that appear healthy to the casual observer but that are, in fact, devoid of terrestrial arthropods and the ecosystem functions that they support. For this reason, we encourage the further study of terrestrial arthropods as a useful indicator of marsh health following oil spills or other environmental impacts (Campbell and Denno 1976, Barnby et al. 1985).

AcknowledgmentsWe thank the National Science Foundation (for grants no. OCE10-45221, no. OCE06-20959, no. DEB-1044599), the Gulf of Mexico Research Initiative Coastal Waters Consortium, and the Northern Gulf Institute for financial support. This work is a contribution of the Georgia Coastal Ecosystems program, part of the Long Term Ecological Research Network. The financial sources supporting this research had no role in the design or execution of the study, the data analysis, the decision to publish, or manuscript preparation. We thank two anonymous reviewers for helpful comments that improved the manuscript.

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Steven C. Pennings ([email protected]) and Brittany D. McCall are affiliated with the Department of Biology and Biochemistry at the University of Houston, in Houston, Texas. Linda Hooper-Bui is affiliated with the Department of Environmental Science in the School of Coast and Environment at Louisiana State University, in Baton Rouge.



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Effects of Oil Spills on Terrestrial Arthropods in Coastal Wetlandsnsmn1.uh.edu/steve/CV/Publications/Pennings et al 2014... · 2014-09-02 · Terrestrial arthropods provide valuable